Surplus and stress control autumn timing

Christine R. Rollinson

Science 27 Nov 2020:

Vol. 370, Issue 6520, pp. 1030-1031

DOI: 10.1126/science.abf4481

无论是秋季衰老的驱动因素，温带落叶林的潜在生产力并不是无限的。研究表明，单靠森林固碳（Forest carbon sequestration）不能与人为碳排放或气候变化保持同步，这意味着森林碳汇的有限性还没有完全被理解。因此，尽管树木和森林仍然是减轻气候变化影响的一种解决办法，但它们不能成为应对气候变化的唯一手段。包括减排、树木养护和种植在内的各种气候行动组合对于减轻人为碳排放和气候变化至关重要。

Trees of the Teutoburg Forest in Lower Saxony, Germany, display colors of autumn leaf senescence.

The presence of leaves on deciduous trees not only marks the changing of the seasons, but also defines the period of time in which trees store carbon from the air in leaves, wood, and roots. Warming winters causing earlier spring-leaf emergence is a widespread pattern of climate-change impacts across temperate tree species and their locations (1). Much more idiosyncratic is the timing of leaf senescence (deterioration), which offers no clear indication of whether future warming will cause an extended autumn growing season that leads to greater carbon-storage potential (2). On page 1066 of this issue, Zani et al. (3) demonstrate that there might be limits to how much carbon a tree can use or store in a single year. Further, if all carbon needs are met, leaves might senesce earlier rather than later in the autumn.

Leaf shedding at the end of the growing season in cold-temperate regions is an evolutionary adaptation to acute stressors (such as freezing temperatures and a lack of moisture available in frozen soils), which often limit species' survival and geographic distributions (4, 5). The mechanistic impacts of mortality-inducing events on trees have likely contributed to senescence being commonly portrayed through a stress-based, supply-side framework. From the photosynthetic carbon supply perspective, leaves become a liability rather than an asset to a tree when the leaves do not have the available resources to be net carbon producers. This explains early leaf loss and mortality in response to stressors such as drought or heat (6, 7). The well-understood role of leaves as carbon suppliers to the tree forms the basis for the common assumption that alleviating plant stress will allow leaves to persist and trees to continue storing carbon for a longer time period in the autumn.

The new work of Zani et al. demonstrates that focusing only on carbon supply is a flawed line of investigation because it entails the assumption that photosynthesis can be sustained indefinitely so long as resources are available, and thus, that senescence is triggered solely by photosynthetic limiters (such as short days or cold temperatures). Zani et al. revealed this shortcoming by demonstrating with observational, experimental, and modeling evidence that increased growing-season productivity can lead to earlier, rather than later, leaf senescence in temperate trees. These findings build on a growing body of literature focused on the demand side of the carbon cycle, in which growth and productivity are limited by the ability of different tissues, such as roots or stems, to use and store carbon (carbon “sinks”).

In particular, sink limitation has been highlighted as a mechanism to explain the hotly debated lack of a clear carbon fertilization effect on tree growth. Carbon fertilization hypotheses are typically supply focused: Increasing atmospheric carbon from anthropogenic emissions increases the carbon available for plant photosynthesis, making carbon movement into leaves more efficient. Although carbon-enrichment studies and analyses of carbon isotopes stored in tree rings provide evidence for an increase in the efficiency of plant photosynthesis with increased atmospheric carbon, there is limited evidence that this translates into increased long-term tree growth and forest carbon storage (8). If more carbon is unnecessary because the other requirements for biological activity in sink tissues are met, trees will fail to grow more rapidly in response to additional carbon. From this demand-side perspective, leaves become unneeded and consequently senesce when the carbon they would fix in photosynthesis has nowhere to go because the available sinks are no longer taking more carbon.

Sink-limitation frameworks often lack mechanistic processes that cause various tissues or functions to no longer use or store carbon. Sink limitation can be an outcome of low productivity and allocation to tissues such as roots or wood that store carbon (9). However, in other cases, a highly productive early season can result in the production of an unsustainably large leaf area that leads to late-season stress and subsequent early senescence (10). Sink-based limitation from lack of carbon demand also might simply be the result of asynchronous tissue phenology arising from independent environmental controls on biological activity in different parts of a plant. For example, root growth in many, if not most, species occurs asynchronously with leaf production (11). When root and wood activity cease to use or store carbon, those tissues become unavailable as carbon sinks. Thus, leaves become costly to maintain, not because of their decreased carbon productivity potential but because there is no room for the carbon they make. Unavailability of potential sinks gives the tree a carbon economic incentive to senesce early despite suitable environmental conditions for photosynthesis.

In the end, the timing of leaf senescence and the autumn season is unlikely to be universally controlled by carbon source or sink dynamics alone (12). In portions of the temperate biome where warm summers increase photosynthesis (as is the case in Zani et al.) and climate change is projected to benefit plant growth, more sink-based limitation of forest productivity seems likely. In regions where stress from heat or low moisture currently causes marked declines in productivity, source-based models might adequately explain autumn leaf senescence. Given the geographic and temporal variability in limitations on tree productivity (13), it is reasonable to expect that the controls on autumn senescence across the temperate biome are likely to include a range from sink-based to source-based limitation. The sink-based models shown to perform well in Zani et al. improve the prediction of autumn senescence in some regions, but the universality of this pattern remains unknown.

Regardless of the drivers of autumn senescence, the potential productivity of temperate deciduous forests is not infinite. Forest carbon sequestration alone cannot be expected to keep pace with anthropogenic carbon emissions or climate change (14). The study of Zani et al. shows that the forest carbon sink is limited in ways that are not yet fully understood. Thus, whereas trees and forests remain one solution for mitigating the impacts of climate change, they cannot be the sole means of climate change response. A diverse portfolio of climate actions that include emissions reductions and tree conservation and planting is essential to mitigate anthropogenic carbon emissions and climate change.

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